Croaking Science: Cave Salamanders

Cave salamanders

Cave salamanders belonging to the amphibian genera Hydromantes and Eurycea occur in southern Europe and widely across the United States. There are at least 11 species of salamander which spend their entire lives in cave environments and many more which complete part of their life-cycle in underground environments e.g. fire salamander (Salamandra salamandra). Many salamanders which live in cave environments exhibit two key characteristics: lack of lungs and direct development (i.e. loss of aquatic larval stage). Having no lungs forces these salamanders to rely on absorbing oxygen across their skin and use bucco-pharangeal breathing, which is obtaining oxygen through the moist lining of the mouth. This type of breathing can only occur effectively in specific conditions of high moisture and cool temperature, which are often found in cave environments. Due to their underground existence, the ecology and behaviour of cave salamanders is poorly understood and recent research is only just beginning to understand the biology of these species.

Previous research on cave salamanders of the genus Hydromantes in southern Italy has shown that these salamanders may reproduce at any time of year, being unconstrained by seasonal environmental changes that affect most non-cave dwelling species. It appears that in most species the female lays a small number of large eggs and protects them until hatching, guarding them from predators and preventing fungal infections (Figure 2). However, the detail of reproductive behaviours such as the number of breeding attempts and nest site selection remain unknown. Recently, Lunghi et al. (2018) carried out a four year study into cave salamanders within the genus Hydromantes at 150 sites in southern Italy. Lunghi et al. (2018) found that in several Hydromantes species the females may retain eggs for many months before releasing them, confirming that the large eggs require a long time to mature in the female before laying. This is followed by a period of at least 6 months of attending eggs and then parental care post-hatching. Therefore, these species require at least two years to complete one reproductive cycle. Given a life-span of only 11 years and maturity at 3-4 years of age, this restricts the number of available reproductive attempts by each female and limits population growth, which is of concern in threatened or vulnerable species. Lunghi et al. (2018) also found that nest site selection was extremely important and that each cave only had a limited number of suitable sites for nesting. Females would occupy only a small number of sites which would vary depending on the year and environmental conditions. This is supported by Lunghi et al. (2014) who found that the wrong choice of nest site can cause breeding failure. Successful breeding seems to occur in nest sites that have high humidity and low temperature. On a yearly basis, different females may use the same nesting site since suitable nests are highly limited. This further suggests that in some species population growth may be limited by suitable areas to breed.

Living in cave environments can be challenging for salamanders as often prey densities are low. Relying on freshwater invertebrates may not always provide enough nutrition for species inhabiting these environments. Recent research by Fenolio et al. (2006) has shown that the Ozark Blind Cave Salamander (Eurycea spelaea) exploits another, less obvious food source. During a study to investigate the community ecology of bat caves in Oklahoma, USA, they found to their surprise that the larval salamanders were consuming bat guano. Initially the researchers thought that the ingestion of guano was incidental since consumption of non-food items in amphibians usually only occurs by accident whilst consuming their normal invertebrate prey. Fenolio et al. (2006) investigated this further and found that the salamanders were actually deliberately ingesting the bat guano as a food source. Nutritional analyses of bat guano revealed that it contained nutrients roughly equivalent to those that would be found in a potential prey item in this ecosystem, amphipods. The researchers also found that numbers of E. spelaea increased significantly in the main parts of the cave system where grey bats deposit fresh guano. This study contradicts the general understanding that salamanders are strictly carnivorous and shows that this adaptation enhances the survival of this species in this harsh environment.

Cave salamanders may also exhibit several morphological adaptations to living in dark and humid underground environments. The Ozark Blind Cave Salamander is also unique in that it starts life as a fully sighted larva but then metamorphoses underground into a terrestrial adult that loses its pigment and becomes blind, with the eyelids eventually fusing (AmphibiaWeb, 2016). There are several hypotheses to explain the reason for this morphological change. However, the most favoured is the energy economy hypothesis which states that the cost of developing and maintaining eyes is substantial and a large portion of the brain is needed for visual processing with high oxygen consumption rates. Energy savings from the loss of eyes could reduce the amount of time needed for foraging and allow energy to be re-invested into other physiological processes, including reproduction (AmphibiaWeb, 2016). In addition, eye loss may be linked to the process of skull development which is a pattern also observed in blind cavefish.

Cave salamanders are a unique group of amphibians with highly evolved ecology and life history characteristics. Unfortunately, an increasing number of cave salamanders are now threatened and classified as Vulnerable or Endangered on the IUCN Red List. Increasing our understanding of the ecology and biology of these declining species is critical in developing effective conservation initiatives, especially in cave environments which are prone to human-induced and climatic change.

References

AmphibiaWeb (2016) Eurycea spelaea: Grotto Salamander <http://amphibiaweb.org/species/4220> University of California, Berkeley, CA, USA. Accessed 27 September, 2019.

Fenolio, D.B., Graening, G.O., Collier, B.A. & Stout, J.F. (2006) Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses. Proceedings of the Royal Society, London B, 273: 439–443.

Lunghi, E., Manenti, R., Manca, S., Mulargia, M., Pennati, R. & Ficetola, G.F. (2014). Nesting of cave salamanders (Hydromantes flavus and H. italicus) in natural environments. Salamandra, 50 (2): 105-109.

Lunghi, E., Corti, C., Manenti, R., Barzaghi, B., Buschettu, S., Canedoli, C., Cogoni, R., De Falco, G., Fais, F., Manca, A., Mirimin, V., Mulargia, M., Mulas, C., Muraro, M., Murgia, R., Veith, M. & Ficetola, G.F. (2018) Comparative reproductive biology of European cave salamanders (genus Hydromantes): nesting selection and multiple annual breeding. Salamandra, 54 (2): 101-108.